Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses

Journal of Neuroscience

Volumn 26, Issue 26, 2006, Pages 7071-7081

  Scott, Ricardo ^a   Rusakov, Dmitri A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

CA3; Calcium; Hippocampus; Presynaptic regulation; Synaptic plasticity; Synaptic transmission

Indexed keywords

CALCIUM ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; CALCIUM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE POTENTIAL; EVOKED RESPONSE; FACILITATION; GRANULE CELL; HIPPOCAMPUS; MALE; MOLECULAR DYNAMICS; MOSSY FIBER; NERVE CELL PLASTICITY; NERVE FIBER; NERVE POTENTIAL; NONHUMAN; PRESYNAPTIC MEMBRANE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PYRAMIDAL NERVE CELL; RAT; SPIKE WAVE; SYNAPSE; SYNAPTIC TRANSMISSION; WHOLE CELL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; ELECTROPHYSIOLOGY; IN VITRO STUDY; KINETICS; METABOLISM; OSMOLARITY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPTOSOME; TIME;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; ELECTROPHYSIOLOGY; KINETICS; MALE; MODELS, NEUROLOGICAL; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; OSMOLAR CONCENTRATION; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 33745932961     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0946-06.2006     Document Type: Article

References (65)

1. Acsady L, Kamondi A, Sik A, Freund T, Buzsaki G (1998) GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18:3386-3403.
2. Alle H, Geiger JD (2006) Combined analog and action potential coding in hippocampal mossy fibers. Science 311:1290-1293.
3. Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. Prog Brain Res 83:1-11.
4. Awatramani GB, Price GD, Trussell LO (2005) Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 48:109-121.
5. 2+ sensor. J Biol Chem 277:16662-16672.
6. 2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22:10593-10602.
7. 2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k- containing terminals. Neuron 38:79-88.
8. Breustedt J, Schmitz D (2004) Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J Neurosci 24:10093-10098.
9. Carter AG, Vogt KE, Foster KA, Regehr WG (2002) Assessing the role of calcium-induced calcium release in short-term presynaptic plasticity at excitatory central synapses. J Neurosci 22:21-28.
10. Chicurel ME, Harris KM (1992) Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 325:169-182.
11. Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206-219.
12. Contractor A, Swanson G, Heinemann SF (2001) Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29:209-216.
13. + channels in hippocampal mossy fiber boutons. Neuron 45:405-417.
14. Engelman HS, MacDermott AB (2004) Presynaptic ionotropic receptors and control of transmitter release. Nat Rev Neurosci 5:135-145.
15. 2+-indicator dyes. Cell Calcium 27:97-106.
16. + channels in hippocampal mossy fiber boutons. Neuron 28:927-939.
17. Griffith WH (1990) Voltage-clamp analysis of posttetanic potentiation of the mossy fiber to CA3 synapse in hippocampus. J Neurophysiol 63:491-501.
18. Helmchen F, Borst JG, Sakmann B (1997) Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471.
19. Henze DA, Wittner L, Buzsaki G (2002) Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5:790-795.
20. Holcman D, Korkotian E, Segal M (2005) Calcium dynamics in dendritic spines, modeling and experiments. Cell Calcium 37:467-475.
21. Jackson MB (1992) Cable analysis with the whole-cell patch clamp. Theory and experiment. Biophys J 61:756-766.
22. Jackson MB, Redman SJ (2003) Calcium dynamics, buffering, and buffer saturation in the boutons of dentate granule-cell axons in the hilus. J Neurosci 23:1612-1621.
23. 2+ influx at the hippocampal mossy fiber synapses. J Neurosci 22:9237-9243.
24. Koester HJ, Johnston D (2005) Target cell-dependent normalization of transmitter release at neocortical synapses. Science 308:863-866.
25. Koester HJ, Sakmann B (2000) Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J Physiol (Lond) 529:625-646.
26. Lauri SE, Bortolotto ZA, Bleakman D, Ornstein PL, Lodge D, Isaac JTR, Collingridge GL (2001) A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 32:697-709.
27. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39:327-341.
28. Lawrence JJ, McBain CJ (2003) Interneuron diversity series: containing the detonation-feedforward inhibition in the CA3 hippocampus. Trends Neurosci 26:631-640.
29. Liang Y, Yuan LL, Johnston D, Gray R (2002) Calcium signaling at single mossy fiber presynaptic terminals in the rat hippocampus. J Neurophysiol 87:1132-1137.
30. Maravall M, Mainen ZF, Sabatini BL, Svoboda K (2000) Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78:2655-2667.
31. Mata AM, Sepulveda MR (2005) Calcium pumps in the central nervous system. Brain Res Brain Res Rev 49:398-405.
32. Matveev V, Zucker RS, Sherman A (2004) Facilitation through buffer saturation: constraints on endogenous buffering properties. Biophys J 86:2691-2709.
33. 2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol (Lond) 547:665-689.
34. 2+ concentration in the store lumen. EMBO J 17:435-442.
35. Mori M, Abegg MH, Gahwiler BH, Gerber U (2004) A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431:453-456.
36. Mori-Kawakami F, Kobayashi K, Takahashi T (2003) Developmental decrease in synaptic facilitation at the mouse hippocampal mossy fibre synapse. J Physiol (Lond) 553:37-48.
37. 2+ microdomains in hippocampal neurons. J Neurosci 25:558-565.
38. 2+. Biophys J 79:3009-3018.
39. Naraghi M (1997) T-jump study of calcium binding kinetics of calcium chelators. Cell Calcium 22:255-268.
40. ++ signals. Cell Calcium 24:345-357.
41. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5:657-664.
42. 2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol (Lond) 547:333-348.
43. Pelkey KA, Lavezzari G, Racca C, Roche KW, McBain CJ (2005) mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46:89-102.
44. Regehr WG, Delaney KR, Tank DW (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14:523-537.
45. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol (Lond) 531:807-826.
46. Ruiz A, Fabian-Fine R, Scott R, Walker MC, Rusakov DA, Kullmann DM (2003) GABAA receptors at hippocampal mossy fibers. Neuron 39:961-973.
47. 2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron 37:287-297.
48. 2+ current modulation by mGluRs at individual hippocampal synapses. Cereb Cortex 14:748-758.
49. 2+ entry by AMPA receptors at individual GABAergic synapses in the cerebellum. J Neurosci 25:4930-4940.
50. Sabatini BL, Regehr WG (1998) Optical measurement of presynaptic calcium currents. Biophys J 74:1549-1563.
51. 2+ ions in dendritic spines. Neuron 33:439-452.
52. Schmitz D, Frerking M, Nicoll RA (2000) Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27:327-338.
53. Schmitz D, Mellor J, Nicoll RA (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976.
54. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893.
55. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
56. Scimemi A, Fine A, Kullmann DM, Rusakov DA (2004) NR2B-containing receptors mediate cross talk among hippocampal synapses. J Neurosci 24:4767-4777.
57. 2+ entry. EMBO J 21:622-630.
58. Tamamaki N, Nojyo Y (1991) Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. J Comp Neurol 303:435-442.
59. Toth K, Suares G, Lawrence JJ, Philips-Tansey E, McBain CJ (2000) Differential mechanisms of transmission at three types of mossy fiber synapse. J Neurosci 20:8279-8289.
60. Turecek R, Trussell LO (2001) Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411:587-590.
61. Verkhratsky A (2005) Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201-279.
62. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53-64.
63. Zalutsky RA, Nicoll RA (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248:1619-1624.
64. Zipfel WR, Webb WW (2001) In vivo diffusion measurements using multiphoton excitation fluorescence photobleaching recovery and fluorescence correlation microscopy. In: Methods in cellular imaging (Periasamy A, ed), pp 216-235. Oxford: Oxford UP.
65. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.